Organization of the mitochondrial genomes of whiteflies, aphids, and psyllids (Hemiptera, Sternorrhyncha)

Thao ML, Baumann L, Baumann P -
(2004)

Bottom Line:
PCR amplification spanning from COIII to genes outside the inserted region and sequence determination of the resulting fragments, indicated that different whitefly species could be placed into one of these arrangement types.A phylogenetic analysis of 19 whitefly species based on genes for mitochondrial cytochrome b, NADH dehydrogenase subunit 1, and 16S ribosomal DNA as well as cospeciating endosymbiont 16S and 23S ribosomal DNA indicated a clustering of species that corresponded to the gene arrangement types.In whiteflies, the region of the mitochondrial genome consisting of genes encoding for COIII-tRNAgly-ND3-tRNAala-tRNAarg-tRNAasn can be transposed from its ancestral position to four different locations on the mitochondrial genome.

Background: With some exceptions, mitochondria within the class Insecta have the same gene content, and generally, a similar gene order allowing the proposal of an ancestral gene order. The principal exceptions are several orders within the Hemipteroid assemblage including the order Thysanoptera, a sister group of the order Hemiptera. Within the Hemiptera, there are available a number of completely sequenced mitochondrial genomes that have a gene order similar to that of the proposed ancestor. None, however, are available from the suborder Sternorryncha that includes whiteflies, psyllids and aphids.

Results: We have determined the complete nucleotide sequence of the mitochondrial genomes of six species of whiteflies, one psyllid and one aphid. Two species of whiteflies, one psyllid and one aphid have mitochondrial genomes with a gene order very similar to that of the proposed insect ancestor. The remaining four species of whiteflies had variations in the gene order. In all cases, there was the excision of a DNA fragment encoding for cytochrome oxidase subunit III(COIII)-tRNAgly-NADH dehydrogenase subunit 3(ND3)-tRNAala-tRNAarg-tRNAasn from the ancestral position between genes for ATP synthase subunit 6 and NADH dehydrogenase subunit 5. Based on the position in which all or part of this fragment was inserted, the mitochondria could be subdivided into four different gene arrangement types. PCR amplification spanning from COIII to genes outside the inserted region and sequence determination of the resulting fragments, indicated that different whitefly species could be placed into one of these arrangement types. A phylogenetic analysis of 19 whitefly species based on genes for mitochondrial cytochrome b, NADH dehydrogenase subunit 1, and 16S ribosomal DNA as well as cospeciating endosymbiont 16S and 23S ribosomal DNA indicated a clustering of species that corresponded to the gene arrangement types.

Conclusions: In whiteflies, the region of the mitochondrial genome consisting of genes encoding for COIII-tRNAgly-ND3-tRNAala-tRNAarg-tRNAasn can be transposed from its ancestral position to four different locations on the mitochondrial genome. Related species within clusters established by phylogenetic analysis of host and endosymbiont genes have the same mitochondrial gene arrangement indicating a transposition in the ancestor of these clusters.

Figure 1: Unrooted phylogenetic tree showing the relationships of members of the Sternorrhyncha (whiteflies, aphids, and psyllids). The tree is based on mitochondrial cytB, ND2, and 16S rDNA sequences. Maximum likelihood analysis, values at nodes are for bootstrap percentages from 500 replicates, only nodes supported by 70% or greater are shown. * by species name designates the organisms for which the complete mitochondrial sequence has been determined.

Mentions:
Table 1 gives the properties and the accession numbers of the mitochondrial DNA sequences determined in this study. An unrooted phylogenetic tree showing the relationships of whiteflies, psyllids and aphids, based on mitochondrial cytB (partial), ND1, and 16S rDNA is presented in Fig. 1. A similar tree is obtained when the amino acid sequence of CytB (partial) and ND1 is used. The sole difference is the position of Neomaskellia andropogonis which becomes part of the cluster containing Bemisia tabaci, Tetraleurodes acaciae, Aleurochiton aceris, and Trialeurodes vaporariorum. Whiteflies, psyllids and aphids have associations with different primary endosymbionts that are transmitted vertically and are essential for the survival of the insect host [2-6]. The time for the establishment of these endosymbiotic associations and the emergence of the composite organism is generally estimated to be between 100 and 200 million years ago [2]. The representative species chosen for study (Fig. 1) probably span the range of diversity within whiteflies, psyllids, and aphids. The maximum % difference in the DNA sequence of these organisms is 33.5 % for whiteflies, 29.7% for psyllids and 13.1% for aphids suggesting that the rate of mitochondrial sequence change in aphids is considerably less than that in whiteflies and psyllids. Resolution of the order of branching among these insect groups is not possible using mitochondrial sequences, since due to their rapid rate of change they are saturated.

Figure 1: Unrooted phylogenetic tree showing the relationships of members of the Sternorrhyncha (whiteflies, aphids, and psyllids). The tree is based on mitochondrial cytB, ND2, and 16S rDNA sequences. Maximum likelihood analysis, values at nodes are for bootstrap percentages from 500 replicates, only nodes supported by 70% or greater are shown. * by species name designates the organisms for which the complete mitochondrial sequence has been determined.

Mentions:
Table 1 gives the properties and the accession numbers of the mitochondrial DNA sequences determined in this study. An unrooted phylogenetic tree showing the relationships of whiteflies, psyllids and aphids, based on mitochondrial cytB (partial), ND1, and 16S rDNA is presented in Fig. 1. A similar tree is obtained when the amino acid sequence of CytB (partial) and ND1 is used. The sole difference is the position of Neomaskellia andropogonis which becomes part of the cluster containing Bemisia tabaci, Tetraleurodes acaciae, Aleurochiton aceris, and Trialeurodes vaporariorum. Whiteflies, psyllids and aphids have associations with different primary endosymbionts that are transmitted vertically and are essential for the survival of the insect host [2-6]. The time for the establishment of these endosymbiotic associations and the emergence of the composite organism is generally estimated to be between 100 and 200 million years ago [2]. The representative species chosen for study (Fig. 1) probably span the range of diversity within whiteflies, psyllids, and aphids. The maximum % difference in the DNA sequence of these organisms is 33.5 % for whiteflies, 29.7% for psyllids and 13.1% for aphids suggesting that the rate of mitochondrial sequence change in aphids is considerably less than that in whiteflies and psyllids. Resolution of the order of branching among these insect groups is not possible using mitochondrial sequences, since due to their rapid rate of change they are saturated.

Bottom Line:
PCR amplification spanning from COIII to genes outside the inserted region and sequence determination of the resulting fragments, indicated that different whitefly species could be placed into one of these arrangement types.A phylogenetic analysis of 19 whitefly species based on genes for mitochondrial cytochrome b, NADH dehydrogenase subunit 1, and 16S ribosomal DNA as well as cospeciating endosymbiont 16S and 23S ribosomal DNA indicated a clustering of species that corresponded to the gene arrangement types.In whiteflies, the region of the mitochondrial genome consisting of genes encoding for COIII-tRNAgly-ND3-tRNAala-tRNAarg-tRNAasn can be transposed from its ancestral position to four different locations on the mitochondrial genome.

Background: With some exceptions, mitochondria within the class Insecta have the same gene content, and generally, a similar gene order allowing the proposal of an ancestral gene order. The principal exceptions are several orders within the Hemipteroid assemblage including the order Thysanoptera, a sister group of the order Hemiptera. Within the Hemiptera, there are available a number of completely sequenced mitochondrial genomes that have a gene order similar to that of the proposed ancestor. None, however, are available from the suborder Sternorryncha that includes whiteflies, psyllids and aphids.

Results: We have determined the complete nucleotide sequence of the mitochondrial genomes of six species of whiteflies, one psyllid and one aphid. Two species of whiteflies, one psyllid and one aphid have mitochondrial genomes with a gene order very similar to that of the proposed insect ancestor. The remaining four species of whiteflies had variations in the gene order. In all cases, there was the excision of a DNA fragment encoding for cytochrome oxidase subunit III(COIII)-tRNAgly-NADH dehydrogenase subunit 3(ND3)-tRNAala-tRNAarg-tRNAasn from the ancestral position between genes for ATP synthase subunit 6 and NADH dehydrogenase subunit 5. Based on the position in which all or part of this fragment was inserted, the mitochondria could be subdivided into four different gene arrangement types. PCR amplification spanning from COIII to genes outside the inserted region and sequence determination of the resulting fragments, indicated that different whitefly species could be placed into one of these arrangement types. A phylogenetic analysis of 19 whitefly species based on genes for mitochondrial cytochrome b, NADH dehydrogenase subunit 1, and 16S ribosomal DNA as well as cospeciating endosymbiont 16S and 23S ribosomal DNA indicated a clustering of species that corresponded to the gene arrangement types.

Conclusions: In whiteflies, the region of the mitochondrial genome consisting of genes encoding for COIII-tRNAgly-ND3-tRNAala-tRNAarg-tRNAasn can be transposed from its ancestral position to four different locations on the mitochondrial genome. Related species within clusters established by phylogenetic analysis of host and endosymbiont genes have the same mitochondrial gene arrangement indicating a transposition in the ancestor of these clusters.